Skip to main content
Log in

Mechanical signalling, calcium and plant form

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Calcium is a dynamic signalling molecule which acts to transduce numerous signals in plant tissues. The basis of calcium signalling is outlined and the necessity for measuring and imaging of calcium indicated. Using plants genetically transformed with a cDNA for the calcium-sensitive luminescent protein, aequorin, we have shown touch and wind signals to immediately increase cytosol calcium. Touch and wind signal plant cells mechanically, through tension and compression of appropiate cells. Many plant tissues and cells are very sensitive to mechanical stimulation and the obvious examples of climbing plants, insectivorous species as well as other less well-known examples are described. Touch sensing in these plants may be a simple evolutionary modification of sensitive mechanosensing system present in every plant. The possibility that gravitropism may be a specific adaptation of touch sensing is discussed. There is a growing appreciation that plant form may have a mechanical basis. A simple mechanical mechanism specifying spherical, cylindrical and flat-bladed structures is suggested. The limited morphological variety of plant tissues may also reflect mechanical specification. The article concludes with a discussion of the mechanisms of mechanical sensing, identifying integrin-like molecules as one important component, and considers the specific role of calcium.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Allan AC, Fricker MD, Ward J, Beale M, Trewavas AJ: Caged ABA induced calcium transients in guard cells of Commelina communis are dependant on previous growth temperature Plant Cell 6 1319–1328.

  2. Bachs O, Carafoli E: Calmodulin and calmodulin-binding proteins in liver cell nuclei. J Biol Chem 262: 10786–10790 (1987).

    PubMed  Google Scholar 

  3. Barritt GJ: Communication Within Animal Cells. Oxford University Press Oxford (1992).

    Google Scholar 

  4. Bentrup FW: Reception and transduction of electrical and mechanical stimuli. In: Haupt WB, Feinlieb ME (eds) Physiology of Movements. Encyclopedia of Plant Physiology, New Series, vol. 7, pp. 42–70 (1979).

  5. Braam J, Davies RW: Rain-, wind- and touch-induced expression of calmodulin and calmodulin related genes in Arabidopsis. Cell 60: 357–364 (1990).

    Article  PubMed  Google Scholar 

  6. Bunning E: Über die Verhinderung des Etiolements. Ber Deut Bot Ges 59: 2–9 (1941).

    Google Scholar 

  7. Bunning E, Lempnau C: Über die Wirkung mechnischer und photischer Reize auf die Gewebe und Organbildung von Mimosa pudica. Ber Deut Bot Ges 67: 10–18 (1954).

    Google Scholar 

  8. Burridge K, Fath K, Kelly T, Nuckolls G, Turner C: Focal adhesions. Annu Rev Cell Biol 4: 487–525 (1988).

    PubMed  Google Scholar 

  9. Caspar T, Pickard BG: Gravitropism by a starchless mutant of Arabidopsis; implications for the starch statolith theory. Planta 177: 185–197 (1989).

    PubMed  Google Scholar 

  10. Clifford PE, Fensom DS, Munt BJ, McDowell WE: Lateral stress initiates bending responses in dandelion peduncles; a clue to geotropism? Can J Bot 60: 2671–2673 (1982).

    Google Scholar 

  11. Damsky CH, Werb Z: Signal transduction by integrin receptors for extracellular matrix: cooperative processing of extracellular information. Curr Opin Cell Biol 4: 772–781 (1992).

    Article  PubMed  Google Scholar 

  12. Darwin C: The Power of Movement in Plants, John Murray, London (1880).

    Google Scholar 

  13. Darwin C: The Movements and Habits of Climbing Plants. John Murray, London (1891).

    Google Scholar 

  14. Denton RM, McCormack JG, Edyell NJ: Role of calcium ions in the regulation of intramitochondrial metabolism. Biochem J 190: 107–117 (1980).

    PubMed  Google Scholar 

  15. Ding JP, Pickard BG: Mechanosensory calcium selective cation channels in epidermal cells. Plant J 3: 83–110 (1993).

    Article  Google Scholar 

  16. Evans DE, Briars SA, Williams LE: Active calcium transport by plant cell membranes. J Exp Bot 42: 285–303 (1991).

    Google Scholar 

  17. Franklin-Tong VE, Ryde JP, Read ND, Trewavas AJ, Franklin C: The self incompatability response in Papaver rhoeas is mediated by free cytosolic calcium. Plant J 4: 163–177 (1993).

    Article  Google Scholar 

  18. Gilroy S, Bethke PC, Jones RL: Calcium homeostasis in plants. J Cell Sci 106: 453–462 (1993).

    PubMed  Google Scholar 

  19. Gilroy S, Read ND, Trewavas AJ: Elevation of cytosol calcium using caged calcium and caged inostiol phosphate initiates stomatal closure. Nature 346: 769–771 (1990).

    Article  PubMed  Google Scholar 

  20. Gilroy S, Trewavas AJ: Signal sensing and signal transduction across the plasma membrane. In: Larsson C, Moller IM (eds) The Plant Plasma Membrane, pp. 203–233. Springer-Verlag, Heidelberg (1990).

    Google Scholar 

  21. Ginsburg MH, Xiaoping D, Plow EF: Inside-out integrin signalling. Curr Opin Cell Biol 4: 766–771 (1992).

    Article  PubMed  Google Scholar 

  22. Goodner R, Quatrano RS: Fucus embryogenesis: a model to study the establishment of polarity. Plant Cell 5: 1471–1481 (1993).

    Article  PubMed  Google Scholar 

  23. Goodwin BC, Briere C, O'Shea POP: Mechanisms underlying the formation of spatial structure in cells. Soc Gen Microbiol Symp 23: 1–9 (1987).

    Google Scholar 

  24. Goodwin BC, Trainor LEH: Tip and whorl morphogensis in Acetabularia by calcium regulated strain fields. J Theor Biol 117: 79–106 (1985).

    Google Scholar 

  25. Grace J: Plant Response to Wind. Academic Press, London (1977).

    Google Scholar 

  26. Hanson JB, Trewavas AJ: Regulation of plant cell cell growth: the changing perspective. New Phytol 90: 1–18 (1982).

    Google Scholar 

  27. Hirouchi T, Suda S: Thigmotropism in the growth of pollen tubes of Lilium longiflorum. Plant Cell Physiol 16: 377–381 (1975).

    Google Scholar 

  28. Hoch HC, Staples RC, Whitehead B, Comeau J, Wolf ED: Signalling for growth orientation and cell differentiation by surface topography in Uromyces. Science 235: 1659–1662 (1987).

    Google Scholar 

  29. Hynes RO: Integrins: A family of cell surface receptors. Cell 48: 549–554 (1987).

    Article  PubMed  Google Scholar 

  30. Ingber D: Integrins as mechanochemical transducers. Curr Opin Cell Biol 3: 841–848 (1991).

    Article  PubMed  Google Scholar 

  31. Jaffe MJ: Classes and mechanisms of calcium waves. Cell Calcium 14: 736–745 (1993).

    Article  PubMed  Google Scholar 

  32. Jaffe MJ: Thigmomorphogenesis; the response of plant growth and development to mechanical perturbation. Planta 114: 143–157 (1973).

    Google Scholar 

  33. Jones RS, Mitchell CA: Calcium ion involvment in growth inhibition of mechanically-stressed soybean seedlings. Physiol Plant 76: 598–602 (1989).

    PubMed  Google Scholar 

  34. Kirchhofer D, Grzesiak J, Pierschbascher MD: Calcium as a potential physiological regulator of integrin mediated cell adhesion J Biol Chem 266: 4471–4477 (1991).

    PubMed  Google Scholar 

  35. Kiss JZ, Sack FD: Severely-reduced gravitropism in dark grown hypocotyls of a starch deficient mutant of Nicotiania sylvestris. Planta 180: 123–130 (1989).

    PubMed  Google Scholar 

  36. Knight MR, Campbell AK, Smith SM, Trewavas AJ: Transgenic plant aequorin reports the effects of touch and cold shock and fungal elicitors on cytosolic calcium. Nature 352: 524–526 (1991).

    Article  PubMed  Google Scholar 

  37. Knight MR, Smith SM, Trewavas AJ: Wind-induced plant motion immediately increases cytosolic calcium. Proc Natl Acad Sci USA 89: 4967–4972 (1992).

    PubMed  Google Scholar 

  38. Knight MR, Read ND, Campbell AK, Trewavas AJ: Imaging calcium dynamics in living plants using semisynthetic recombinant aequorins. J Cell Biol 121: 83–90 (1993).

    Article  PubMed  Google Scholar 

  39. Kutschera U: The role of the epidermis in the control of elongation growth in stems and coleoptiles. Bot Acta 105: 246–253 (1992).

    Google Scholar 

  40. Lang A: Progressiveness and contagiousness in plant differentiation and development. Encyclopedia of Plant Physiology vol 15 (1), pp. 409–424 (1964).

    Google Scholar 

  41. Linthilac PM, Vesecky TB: Stress-induced alignment of division plane in plant tissues grown in vitro. Nature 307: 363–364 (1984).

    Google Scholar 

  42. Liu Y, Storm DR: Dephosphorylation of neuromodulin by calcineurin. J Biol Chem 264: 12800–12804 (1989). Trends Pharmacol 11: 107–111 (1990).

    PubMed  Google Scholar 

  43. Malho R, Read ND, Pais MS, Trewavas AJ: Role of cytosolic free calcium in the reorientation of pollen tube growth. Plant J 5: 331–341 (1994).

    Google Scholar 

  44. McCormack JG, Halestrap AP, Denton RM: Role of calcium ions in regulation of mammalian intramitochondrial metabolism. Physiol Rev 70: 391–425 (1990).

    PubMed  Google Scholar 

  45. Melkonian B, Burchet M, Kreimer G, Latzko E: Binding and possible function of calcium in the chloroplast. Curr Topics Plant Biochem Physiol 9: 38–46 (1990).

    Google Scholar 

  46. Miller DB, Callahan DA, Gross DJ, Hepler PK: Free Ca2+ gradient in growing pollen tubes of Lilium. J Cell Sci 101: 7–12 (1992).

    Google Scholar 

  47. Neel PL, Harris RW: Motion-induced inhibition of elongation and induction of dormancy in Liquidamber. Science 173: 58–59 (1971).

    Google Scholar 

  48. Neel PL, Harris RW: Growth inhibition by mechanical stress. Science 174: 961–962 (1972).

    Google Scholar 

  49. Neel PL, Harris RW: Tree seedling growth: effect of shaking. Science 175: 918–919 (1972).

    Google Scholar 

  50. Obermeyer G, Weisenseel MH: Calcium channel blocker and calmodulin antagonists affect the gradient of free calcium ions in lily pollen tubes. Eur J Cell Biol 56: 319–327 (1991).

    PubMed  Google Scholar 

  51. Odell GM, Oster G, Alberch P, Burnside B: The mechanical basis of morphogenesis. Devel Biol 85: 446–462 (1981).

    Google Scholar 

  52. Oster GF, Murray JD, Harris AK: Mechanical aspects of mesenchymal morphogenesis. J Embryol Exp Morphol 78: 83–125 (1983).

    PubMed  Google Scholar 

  53. Pfeffer W: The Physiology of Plants, vol 3 (translated by A.J. Ewart). Clarendon Press, Oxford (1906).

    Google Scholar 

  54. Pickard BD, Ding JP: Gravity sensing by higher plants. Adv Comp Envir Physiol 10: 81–110 (1992).

    Google Scholar 

  55. Poovaiah BW, Reddy ASN: Calcium and signal transduction in plants. Crit Rev Plant Sci 12: 185–211 (1993).

    PubMed  Google Scholar 

  56. Rathore KS, Cork RJ, Robinson KR: A cytoplasmic gradient of Ca2+ is correlated with the growth of lily pollen tubes. Devel Biol 148: 612–619 (1991).

    Google Scholar 

  57. Sanders LC, Wang CS, Walling LL, Lord EM: A homolog of the substrate adhesion factor vitronectin occurs in four species of flowering plants. Plant Cell 3: 629–635 (1991).

    PubMed  Google Scholar 

  58. Schindler M, Meiners S, Cheresh DA: RGD-dependent linkage between plant cell wall and plasma membrane; consequences for growth. J Cell Biol 108: 1955–1965 (1989).

    PubMed  Google Scholar 

  59. Selker JML, Steucek GL, Green PB: Biophysical mechanisms for morphogenetic progressions at the shoot apex. Devel Biol 153: 29–43 (1992).

    Google Scholar 

  60. Shacklock P, Read ND, Trewavas AJ: Cytosolic free calcium mediates red light induced photomorphogeneis. Nature 358: 753–755 (1992).

    Google Scholar 

  61. Shankar G, Davison I, Helfrich MP, Mason WT, Horton MA. Integrin receptor mediated mobilisation of intranuclear calcium in rat osteoclasts. J Cell Sci 105: 61–68 (1993).

    PubMed  Google Scholar 

  62. Sinclair W, Oliver I, Maher P, Trewvas AJ: Effect of gravistimulation on calmodulin mRNA in wild type and mutant Arabidopsis plants. Plant Physiol, submitted (1994).

  63. Stark P: Weitere Untersuchungen über das Restantengesetz beim Haptotropismus. Jahrb Wiss Bot 61: 126–167 (1921).

    Google Scholar 

  64. Stinemetz CL, Kuzmanoff KM, Evans ML, Jarret HW: Correlations between calmodulin activity and gravitropic sensitivity in primary roots of maize. Plant Physiol 84: 1337–1342 (1987).

    PubMed  Google Scholar 

  65. Thompson DA: On Growth and Form. Cambridge University Press, Cambridge, UK (1942).

    Google Scholar 

  66. Trewavas AJ: How do plant growth substances work? Plant Cell Envir 4: 203–228 (1981).

    Google Scholar 

  67. Trewavas AJ: How do plant growth substances work? II. Plant Cell Envir 14: 1–12 (1991).

    Google Scholar 

  68. Trewavas AJ, Knight MR: The regulation of shape and form by cytosolic calcium. In: Ingram D, Hudson A (eds) Shape and Form in Plant and Fungal Cells, pp. 221–233. Academic Press, London (1992).

    Google Scholar 

  69. Wagner VT, Brian L, Quatrano RS: Role of a vitronectinlike molecule in embryo adhesion of the brown alga Fucus. Proc Natl Acad Sci USA 89: 3644–3648 (1992).

    PubMed  Google Scholar 

  70. Wang N, Butler JP, Ingber D: Mechanotransduction across the cell surface and through the cytoskeleton. Science 260: 1124–1127 (1993).

    PubMed  Google Scholar 

  71. Wayne R, Staves MP, Leopold AC: Gravity dependent polarity of cytoplasmic streaming in Nitellopsis. Protoplasma 155: 43–57 (1990).

    PubMed  Google Scholar 

  72. Wyatt SE, Carpita NC: The plant cytoskelton-cell wall continuum Trends Cell Biol 3: 413–417 (1993).

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Trewavas, A., Knight, M. Mechanical signalling, calcium and plant form. Plant Mol Biol 26, 1329–1341 (1994). https://doi.org/10.1007/BF00016478

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00016478

Key words

Navigation